Abstract
Ancient evolutionary events are difficult to study because their current products are derived forms altered by millions of years of adaptation. The primary endosymbiotic event formed the first photosynthetic eukaryote resulting in both plants and algae, with vast consequences for life on Earth. The evolutionary time that passed since this event means the dominant mechanisms and changes that were required are obscured. Synthetic symbioses such as the novel interaction between Paramecium bursaria and the cyanobacterium Synechocystis PC6803, recently established in the laboratory, permit a unique window on the possible early trajectories of this critical evolutionary event. Here, we apply metabolic modelling, using flux balance analysis (FBA), to predict the metabolic adaptations necessary for this previously free-living symbiont to transition to the endosymbiotic niche. By enforcing reciprocal nutrient trading, we are able to predict the most efficient exchange nutrients for both host and symbiont. During the transition from free-living to obligate symbiosis, it is likely that the trading parameters will change over time, which leads in our model to discontinuous changes in the preferred exchange nutrients. Our results show the applicability of FBA modelling to ancient evolutionary transitions driven by metabolic exchanges, and predict how newly established endosymbioses, governed by conflict, will differ from a well-developed one that has reached a mutual-benefit state.
Highlights
Endosymbiosis, a symbiotic relationship where one organism resides within another, has led to some of the most important transitions in the evolution of eukaryotes, including their origin and later the formation of photosynthetic eukaryotes [1]
Endosymbiosis is a common occurrence in algae, though the evolutionary transition of photosynthetic symbionts into organelles is rare [8]
Endosymbionts satisfy more of the assumptions of flux balance analysis (FBA) modelling than other organisms, because the host provides a stable environment for the symbiont permitting a context with less fluctuation in gene expression
Summary
Endosymbiosis, a symbiotic relationship where one organism resides within another, has led to some of the most important transitions in the evolution of eukaryotes, including their origin and later the formation of photosynthetic eukaryotes [1]. Genome reduction over the course of coevolution between host and endosymbiont is frequently accompanied by gene transfer from plastid to host nucleus, as has occurred in plants with the small subunit of the primary enzyme of carbon fixation ribulose-1,5bisphosphate carboxylase/oxygenase (rbcS) encoded by the nuclear rather than the plastid genome with the large subunit, rbcL, remaining encoded by the plastid [10,11,12]. This highly derived form makes the establishment of this major endosymbiotic event difficult to study
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